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Food web dynamics in open and closed systems
Johan Lövgren
2004
Department of Ecology and Environmental ScienceUmeå University SE - 90187 Umeå
Sweden
AKADEMISK AVHANDLING
Som med vederbörligt tillstånd av rektorsämbetet vid Umeå Universitet förerhållande av filosofie doktorsexamen i ekologi kommer att offentligenförsvaras fredagen den 28:e maj, 2004, kl. 13.00 i Stora Hörsalen, KBC.
Examinator: Professor Lennart Persson, Umeå UniversitetOpponent: Professor Jonathan Chase, Washington, University In St. Louis, USA
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ISBN: 91-7305-662-6 Printed by Solfjädern Offset AB © Johan Lövgren 2004
Organisation Document nameUmeå Unversity Doctoral DissertationAnimal EcologyDept. of Ecology and Environmental Science Date of IssueSE – 901 87 Umeå, Sweden May 2004
Author: Johan Lövgren
Title: Food web dynamics in open and closed systems
AbstractMost food webs in nature are open, and influenced by processes outside the focal habitat. The impactof an allochtonous subsidy on the dynamics in the recipient food web depends both on the trophicrole of the recipient, and on heterogeneity within trophic levels. Heterogeneity within trophic levelsallows for compensatory responses, as a decrease in one species can be compensated by an increase inanother species at the same trophic level.
This thesis is a summary of enclosure and microcosm experiments that aimed to study theimpact of allochtonous subsidies on food web dynamics in a heterogeneous food web. In theenclosure studies, a three trophic level littoral food web was used. The predator in the food web,young of the year (YOY) perch, can potentially affect two pathways in the in the food web, connectedto the two growth forms of primary producer; phytoplankton and periphyton, and the associatedherbivores to each of them; filtering and scraping herbivores. Manipulation of the openness for thedifferent trophic levels to utilize the adjacent habitat showed that the inflow of phytoplankton andcross-habitat foraging by the herbivore level reinforced the compensatory response between the twogrowth forms of primary producers. Allowing YOY perch to utilize the adjacent habitat did not,however, affect the interactions within the food web, as the predation risk imposed by top predatorsin the adjacent natural lake habitat restricted the YOY perch to the littoral habitat.
In the microcosm experiment, the response of an herbivore food web and a microbialcommunity to inflow of resources and food web configuration was studied, using a model littoralfood web. The model food web consisted of two forms of primary producers, i.e. phytoplankton andperiphyton, and two herbivores, i.e. Daphnia pulex feeding on phytoplankton, and Chydorussphaericus feeding on both periphyton and phytoplankton. Three different food web configurations,all having the phytoplankton and periphyton, but either one of the herbivores, or both, were set up.The flow regimes consisted of an open treatment receiving a constant supply of phytoplankton, and aclosed treatment with an initial resource pool, but no additional external input. The effect of theinflow of phytoplankton on the other organisms in the food web was clearly affected by the food webconfiguration. In the presence of D. pulex, the inflow of phytoplankton was made accessible toperiphyton, and indirectly to C. sphaericus, which increased to such high densities that D. pulex wasnegatively affected. The inflow of phytoplankton had an indirect negative effect on the microbialcommunity, since the biomass of herbivores increased, which imposed a higher grazing pressure onall parts of the microbial community.
Key words: Allochtonous input, cross-habitat foraging, donor control, heterogeneity within trophiclevel, compensation, food web, littoral
Language: English ISBN: 91-7305-662-6 Number of pages: 30+ 5papers
Signature: Date: 26 April2004
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TillSara och Irma
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TABLE OF CONTENTS
Introduction……………………………………………………………….6
System studied: The lake ecosystem…………………………………….9
Food webs studied………………………………………………..………11
The impact of allochtonous inputs and cross habitat
foraging in food webs……………………………………………...…….13The impact of predation in an open littoral food web (I)………...……….13The impact of predation in an open and closed food web (II)……….........14
Impact of behaviorally induced habitat
shifts on food web dynamics (III)……………………………….…………17
Allocthonous input and food web configuration…………………….…18
Allocthonous input and different food web configurations:
Responses of the herbivore food web (IV)………………………………....19
Allocthonous input and different food web configurations:
Responses of the microbial community (V)…………………………….….21
Concluding remarks…………………………………………………..….22
Acknowledgments………………………………………….……………..23
References……………………………………………………...…………23
Appendices: Papers I-V
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- LIST OF PAPERS -
This thesis is a summary and discussion of the following papers that will bereferred to in the text by their Roman numerals.
I. Lövgren, J. and Persson, L. 2002. Fish mediated indirect effects in littoral food web. Oikos 96: 150-156.
II: Lövgren, J. Allochtonous input and cross-habitat foraging: impact ontrophic interactions in a littoral food web. Submitted manuscript
III. Lövgren, J., Bertolo, A. and Persson L. Flexible behavior at differenttrophic levels: impact on trophic dynamics in a littoral food web.Manuscript
IV. Lövgren, J. Reinikainen M. and Persson L. Allochtonous input andtrophic level heterogeneity: impact on an aquatic food web.Submitted manuscript
V. Reinikainen, M., Lövgren J. and Persson L. Associations betweenthe microbial community and metazoan grazers as affected byallochtonous resources in aquatic microcosms. Manuscript
Paper I is reproduced with the permission from the publisher.
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Food web dynamics in open and closed systems
Introduction
The basic concept on which a substantial part of the discussion on trophic
interactions has focused is the Exploitation Ecosystem Hypothesis (EEH)
(Oksanen et al. 1981, Hairston and Hairston 1993, Persson et al. 1996,
Persson 1999). EEH in its original form assumes that a food web can be
aggregated into a food chain where each trophic level acts as one single unit
(Oksanen et al. 1981). The model by Oksanen et al. (1981) predicts that the
equilibrium biomass of adjacent trophic levels would be unrelated to each
other, whereas trophic levels two steps apart would be positively related to
eachother with increasing productivity. Although both comparative and
experimental evidence suggest that enrichment may lead to patterns
predicted by the model by Oksanen et al. (1981) (Wooton and Power 1995,
Mazumder 1994, Kauntzinger and Morin 1998, Oksanen and Oksanen
2000), it is commonly observed that adjacent trophic levels respond
positively to enrichment (McQueen et al. 1986, Leibold 1989, Hansson et al
1992, Brett and Goldman 1997, Leibold et al.1997, Persson 1997, Mikola
and Setälaä 1998). There are several potential mechanisms for why adjacent
trophic levels would increase in response to an increased productivity, such
as interference among predators (Oksanen et al. 1995) and unstable
predator- prey dynamics (Abrams and Roth 1994, see Persson 1999 for
additional mechanisms). However, the general explanation for these
observation is that heterogeneity within trophic levels (i.e. more than one
species at each trophic level) causes consumer induced changes in the
6
density of one resource species, to be compensated by changes in other
resource species that are less vulnerable to consumption (Leibold 1989,
Hunter and Price 1992, Leibold and Wilbur 1992, Rosemond 1996, Leibold
et al. 1997, Chase 1998, Pace et al.1998, Hansson et al. 1998, Hulot et
al.1999, Bohannan and Lenski 1999, 2000, Steiner 2001, 2003).
Compensatory responses between organisms within a trophic level are likely
to dampen the effects of predators on levels below and thus reduce the
strength of a trophic cascade in terms of total density/biomass changes,
where a trophic cascade is defined as a change in the biomass of the primary
producer, induced by a change of species an even number of links above
(Persson 1999).
An important reason for within trophic level heterogeneity is that
food webs consist of organisms from different habitats. Furthermore,
organisms connect habitats by movements and feeding in the different
habitats (Carpenter and Kitchell 1993, Persson et al. 1996, Polis and Strong
1996, Polis et al. 1997, Persson and Crowder 1997). Most habitats and
systems in nature are connected to each other, and even systems that seem to
be closed are connected to other habitats, and influenced by processes taking
place outside the system under study (Polis and Strong 1996, Polis et al.
1997). The connections between habitats can be due to abiotic factors such
as wind and water movements that transport nutrients and detritus across
habitat borders (Polis et al. 1996, 1997, Barko and James 1997, MacIntyre
and Melack 1995). Mobile consumers may also connect habitats both in
terms of prey consumption and nutrient translocation (Carpenter et al. 1992,
Schindler et al. 1996, Vanni 1996, Jeppesen et al. 1997, Polis et al. 1996,
1997).
Recent papers have argued that input of resources produced outside
the focal habitat (allochtonous input or subsidies) are common in a variety
7
of systems and can be received at any trophic level. Field observations
(Power 1990, Polis and Hurd 1995, Polis et al. 1996, Rose and Polis 1998,
Sabo and Power 2002 a, b, Bustamante et al. 1995, Nakano et al. 1999,
Nakano and Murakami 2001), and theory (De Angelis 1980, Polis et al.
1997, Huxel and McCann 1998, Huxel et al. 2002) have shown that the
population dynamics can be dependent on the allochtonous inputs to the
system, and that effects can propagate through trophic links and indirectly
change the abundance of populations other than the recipient species.
Theoretical studies suggest that the impact of an allocthonous input are
depending on the magnitude of the input and on the trophic level that
receives the input (Polis et al.1996, Huxel and MCann 1998, Huxel et al.
2002). An allochtonous input can in some systems even exceed the total in
situ production and decouple consumers from the renewal rate of its prey,
resulting in donor controlled consumers (De Angelis 1980, Strong 1992,
Persson et al. 1996).
This thesis focused on the impact of allochtonous subsidies on food web
dynamics in a heterogeneous food web, and main questions asked were:
i) Do the trophic interactions in a food web differ depending on which
trophic level that utilizes the adjacent habitat?ii) How is the effect of allochtonous input affected by food web
configuration?
The experiments conducted in order to answer the above questions were
performed at different spatial scales (from aquaria to large sized enclosures
in lakes) and with varied number of species at lower trophic levels (two or
more). The rationale behind this was that field experiments have the
advantage of including many aspects of the complexity of natural systems,
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but on the other hand have the disadvantage of making it difficult to control
for factors such as the form of the allochtonous input and the structure of the
recipient food web. To delineate the effects of these factors, laboratory
experiments are useful, as they will allow a high degree of control over both
the allochtonous input and the structure of the recipient food web.
Systems studied: The lake ecosystem
Lakes are often used as model ecosystems because they are discrete, self
contained ecosystem with clearly defined boundaries, and with identifiable
connections with adjacent habitats (Vander Zanden and Vadeboncoeur
2001, Vadeboncoeur et al. 2002, Schindler and Scheuerell 2002). A lake
itself is however a complex ecosystem composed of at least three different
habitats: the pelagic (open water), the benthic (bottom-associated) and the
littoral (shoreline). These habitats have often been studied as distinct
ecosystems due to the difference in physical structure, productivity and
trophic structure (Lodge et al. 1988, Schindler and Scheurell 2002). Yet,
these habitats are coupled in many ways, and for example, it has long been
recognized that that the littoral and benthic are linked biogeochemically to
the open water of lakes through wind and water movements that translocate
nutrients between the habitats (Wetzel 1979, MacIntyre and Melack 1995,
Barko and James 1997, Blumenshine et al. 1997). Mobile consumers, like
fish and zooplankton, may transport nutrients between habitats in a variety
of ways. Vertical and horizontal migrations of zooplankton link the benthic
and littoral communities with the pelagic habitat (Vanni 1996, Jeppesen et
al. 1997). Fish that feed in one habitat and excrete in another have been
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argued to potentially translocate nutrients between all the habitats within a
lake (Vanni 1996, Schindler et al. 1996, Vander Zanden and Vadebocoeur
2002). The consequences of the habitat couplings are pronounced. This can
be illustrated by fish that induce pelagic trophic cascades, subsidized by
benthic and littoraly derived resources, which allow them to sustain high
population numbers when they have driven their preferred pelagic prey to
low densities (Schindler et al. 1996, Vanni 1996, Schindler and Scheurell
2002). A special case of habitat coupling is based on behavioral responses to
predators. An example of this type of habitat coupling is when piscivorous
fish restrict smaller fish to the littoral vegetated habitats. As a consequence
zooplankton increase in the open water habitat, and prey resources in the
refuge habitat decrease (Carpenter et al. 1987, Turner and Mittelbach 1990).
A similar pattern is when zooplankton are utilizing the vegetated habitat as a
daytime refuge from planktivorous fish, but at night migrate out in the
pelagic where they control the phytoplankton communities, and thereby
truncates the pelagic trophic cascade (Schriver et al. 1995). The above
examples show that habitat coupling in lake ecosystems may create
situations where the dynamics observed in one habitat may be driven by
processes that occur in another habitat (Schindler and Scheurell 2002).
The results and conclusions from paper I-III comes from
experimental studies conducted in two adjacent low productive lakes named
lake Abbortjärn 2 and lake Abbortjärn 3, situated in central Sweden (64 º
29`N, 19º 26 E). The lakes have low humic content and sparse natural
vegetation. Both lakes contain perch (Perca fluviatilis) and Roach (Rutilus
rutilus) in addition Lake Abbortjärn 2 also contains pike (Esox lucius). Both
lakes have been subjected to a structure treatment where 40 % of the
circumference was covered with artificial vegetation of a width of 2 m. The
mats consisted of 1 m long floating lines anchored to the bottom. The
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addition of artificial vegetation increased both the structural complexity and
the food web complexity. The artificial vegetation also allowed for the
development of a second form of primary producer, i.e. epiphytic
algae/periphyton, and the associated consumers, i.e. scraping herbivores.
Food webs studied
The focal food web that I have studied in I- III was a heterogeneous littoral
food web consisting of two principal forms of primary producers, i.e.
phytoplankton and periphyton, and the herbivores associated with each of
them, i.e. filtering herbivores and scraping herbivores (Fig. 1). The
periphyton in the experimental lakes grows on a chemically inert substrate
and competes with phytoplankton of nutrients in the water column. The
predator in the food web young of the year perch, (YOY), (Perca fluviatilis)
affects both filtering herbivores and scraping herbivores (Person et al. 2000).
The two different pathways are connected at the top (YOY perch) and at the
bottom (nutrients). The aquaria experiment IV, V was in essence a simplified littoral
food web where I used single species in each compartment (Fig. 2). The
experiment was performed indoors in a light and temperature controlled
laboratory environment. The focus in IV was to study relationships between the organisms
presented in (Fig. 2) in V we synthesized data on the microbial community
from the experiment in (IV). The microbial community consisted of ciliates
feeding on flagellates, which in turn are feeding on bacteria; in addition
ciliates are able to utilize bacteria. The cladoceran grazers (D. pulex and C.
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sphaericus) could potentially feed on all the organisms in the microbial
community.
Predator
Filtering herbivores Scraping herbivores
Phytoplankton Periphyton
Fig.1. The focal food web studied in the lake system was a littoral food web consisting oftwo primary producers (phytoplankton and periphyton), and the herbivores connected toeach of them (scraping herbivores and filtering herbivores). The filtering herbivoresconsisted mainly of the cladocerans Ceriodaphnia sp. Bosmina sp. and Sida crystalline. Thescraping herbivores in our study consisted of benthic cladocerans (Chydorid sp.) andmacroinverebrates (chironomids and trichopterans). The predator in the system was YOYperch.
Filtering herbivore Scraping herbivore(Daphnia pulex) (Chydorus sphaericus)
Phytoplankton Periphyton(Scenedesmus obtusiusculus) (Nitzschia perminuta)
Fig. 2. The model food web used in the microcosm experiment. In addition to thesesexperimentally controlled components, we also studied the microbial community thatdeveloped during the course of the experiment.
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The impact of allochtonous inputs and cross habitat foraging in food webs
Cross-habitat foraging and inflow of resources to consumers may allow the
consumer to persist at higher densities than is possible in isolated habitats.
Furthermore, the higher consumer densities affect the in situ resources
directly, and community structure indirectly, via food web effects (Polis et
al. 1997). Potentially, a subsidized consumer can either dampen or reinforce
trophic cascades depending on the magnitude of the inflow and which
trophic level receives the input (Polis et al. 1997).
The impact of predation in an open littoral food web (I)
The aim of the experiment in I was to study the effect of predation in a
heterogeneous food web open for the second trophic level (filtering and
scraping herbivores) to potentially be subsidized. (Fig. 3.).
Pred.
Filt. H. Scra.H. Filt. H. Scra.H.
Phyt. Peri. Phyt. Peri.
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A B
Fig. 3. Graphical representation of the food webs studied in I. Predator (Pred), Filteringherbivores (Filt. H.), Scraping herbivores (Scra.H) , Phytoplankton (Phyt) and Periphyton(Peri). The dotted boxes indicate that the organisms were able to move in and out from theenclosures whereas filled boxes indicate that the organisms were enclosed.
We used net enclosures with and without fish in the littoral habitat. The
mesh size of the net allowed the flow of phytoplankton, and filtering and
scraping herbivores between the enclosures and the adjacent habitat (Fig. 3.
A, B). The major results from the experiment were that although YOY perch
reduced filtering and scraping herbivores, the top down effect did not
cascade down to affect the primary producers. We found no difference in
phytoplankton biomass between treatments, despite the large differences in
biomass of filtering herbivores. This suggests that the inflow of
phytoplankton into the enclosures compensated the loss through grazing by
filtering herbivores. The biomass of periphyton was higher in the absence of
fish, resulting in a positive correlation between scraping herbivore and
epiphytic algae biomass. Our results suggest that the positive indirect effect
of nutrient regeneration by filtering herbivores on periphyton was stronger
than the direct negative effect of grazing by scraping herbivores. Thus, when
a consumer in the food web was subsidized, it had a large impact on the
interactions within the food web as the high inflow rate of phytoplankton
allowed a large biomass of filtering herbivores in the fish free treatment to
sustain. This further allowed a high and constant recycling of nutrients to be
utilized by periphyton. The littoral food web that we studied, with two
primary producers of different growth forms, enhances the potential for
compensatory responses.
The impact of predation in an open and closed food web (II)
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The results from (I) suggested that the allochtonous subsidy to the second
trophic level (inflow of phytoplankton) influenced food web dynamics
substantially. The purpose of this experiment was to study if the effect of
fish predation differed in a system without exchange of the surrounding
water (closed). The experimental set up involved an open system identical to
the system in (I) with and without YOY perch (Fig. 3. A, B) and a closed
system, consisting of enclosures covered in plastic, with and without YOY
perch. (Fig. 4. A, B).
Pred.
Filt. H. Scra.H. Filt. H. Scra.H.
Phyt. Peri. Phyt. Peri.
Fig. 4. Graphical representation of the food webs studied in II. Predator (Pred.), Filteringherbivores (Filt. H.), Scraping herbivores (Scra. H), Phytoplankton (Phyt.) and Periphyton(Peri.). The dotted boxes indicate that the organisms were able to move in and out from theenclosures, whereas filled boxes indicate that the organisms were enclosed.
The impact of the predation of YOY perch in the open systems was to a
large extent in correspondence with (I). The highest biomass of filtering and
scraping herbivores was found in the fish free treatment, and
correspondingly also the highest periphyton biomass. In contrast to (I),
where we found that the biomass of phytoplankton was equal between the
fish free and fish treatment, I found in II that the phytoplankton biomass
15
A B
was lower in the open fish free treatment than in the open fish treatment.
This was related to the fact that the biomass of filtering herbivores in II was
five times higher than in (I). This higher biomass of filtering herbivores was
probably due to filtering herbivores migrating into the enclosures.
The impact of predation by YOY perch in the closed system
generally resulted in the same relationship at lower trophic levels between
the fish and fish free treatment as in the open treatment. The highest
biomass of periphyton was, in correspondence with the open treatment, also
found in the closed fish free treatment. The major difference between the
open and closed treatments was that the biomass of filtering herbivores did
not differ between the closed fish free and fish treatment. This can be related
to the fact that an initial high biomass of filtering herbivores in the closed
fish free treatment decreased the phytoplankton to low levels, and that the
closed design disabled inflow of phytoplankton and migration of filtering
herbivores, which might have allowed a high biomass of filtering herbivores
to persist. The higher biomass of periphyton in the closed fish free
treatment, however, suggests that the initial higher biomass of filtering
herbivores resulted in an overall higher positive indirect effect of filtering
herbivores on periphyton growth in the closed fish free treatment than in the
closed fish treatment.
The overall highest biomass of periphyton was found in the open fish
free treatment, suggesting that the compensatory increase in one of the
primary producers (periphyton) was reinforced in the open treatment, due to
the potential for inflow of phytoplankton produced outside the habitat, and
cross habitat foraging by filtering herbivores.
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Impact of behaviorally induced habitat shifts on food web dynamics (III)
The impact of adjacent habitats can include more than allochtonous
subsidies, as the presence of top predators in a specific habitat can induce
prey to shift to low predation risk habitats, in turn inducing strong cascading
effects both in non refuge (Carpenter et al.1987) and in the refuge habitat
(Power et al. 1989). The aim of this experiment was to study how the food
web interactions in the open littoral food web studied in (I, II) (Fig 3.A, B)
was affected by allowing the third trophic level (YOY perch) to flexibly
utilize both the adjacent and the habitat under study. In one of the treatments
that allowed flexible habitat use by YOY perch, we included two top
predators, pike and perch, in the vegetation (Fig. 4. A, B.).
Pred.
Pred. Pred.
Filt. H. Scra.H. Filt. H. Scra.H.
Phyt. Peri. Phyt. Peri.
Fig. 5. Graphical representation of the food webs studied in III.Top predator (Top P),Predator (Pred.), Filtering herbivores (Filt. H.), Scraping herbivores (Scra. H),Phytoplankton (Phyt.) and Periphyton (Peri.). The dotted boxes indicate that the organismswere able to move in and out from the enclosures, whereas filled boxes indicate that theorganisms were enclosed.
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A B
The major result from this study was that the biomass of lower trophic levels
(herbivores and primary producers) was similar in the treatment where YOY
perch was enclosed and the treatments where YOY perch was able to
flexible habitat choice. The similar effects on lower trophic levels suggest in
turn that YOY perch utilized the vegetated habitat extensively to avoid
predation in the pelagic habitat. Additionally, it suggests that the predation
risk in the pelagic was higher than the predation risk imposed by the top
predators enclosed in the vegetation, which in turn could be related to the
low efficiency of the top predators in structurally complex habitats
(Christensen and Persson 1993). The compensatory response between the
two growth forms of primary producers found in (I) and (II) was also
present in this study, as we found a higher biomass of periphyton in the
treatment without YOY, together with a high biomass of filtering
herbivores.
Our results further suggest that the impact on food web dynamics by
allowing the third trophic level (YOY perch) to utilize the adjacent habitat,
did not change the dynamics compared to when the YOY perch was
restricted to the focal habitat due to a high predation risk in the adjacent
habitat.
Allochtonous input and food web configuration
A donor controlled consumers can increase to densities higher than if
supported by in situ production, and inflict a large top down effect on in situ
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prey (Polis et al. 1996, 1997). The overall food web effect by the
allochtonous input depends on both the configuration of the recipient food
web and the trophic role of the allochtonous input (Polis et al. 1997).
Previous experiments have shown that food web configuration and within
trophic level heterogeneity can have substantial effects on patterns of trophic
biomass in response to an increased in situ productivity (Hansson et al.
1998, Leibold and Wilbur 1992, Steiner 2001, 2003, Bohannan and Lenski
1999, 2000, Persson 2001). In IV we studied the effect of food web
configuration and within trophic level heterogeneity in response to a system
where the consumers were partly decoupled from in situ productivity by an
allochtonous input.The microbial community has been argued to be regulated both by
resource levels and by herbivorous cladocerans (Reimann and Christoffersen
1993). Previous studies that have delineated between these processes have
manipulated in situ resources (nutrient addition) and measured the
difference between herbivorous cladoceran grazing and protozoans (ciliates
and flagellates) grazing by means of truncation experiments (Samuelsson et
al. 2002, Samuelsson and Andersson 2003). In V we compared the effect on
the microbial community consisting of ciliates, flagellates and bacteria in an
open system with a system that was depending on in situ productivity. In
addition, we studied how different food web configurations of herbivorous
cladocerans affected the way in which the microbial community responded
to the inflow of resources.
Allochtonous input and different food web configurations:
Response of the herbivore food web ( IV)
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The impact of food web complexity in open and closed food webs was
explored experimentally under controlled laboratory conditions. We used an
aquatic model food web consisting of two forms of primary producers, i.e.
phytoplankton (Scenedesmus obtusiusculus), and periphyton (Nitzschia
perminuta), and two types of consumers, i.e. Daphnia pulex feeding on
phytoplankton and Chydorous sphaericus feeding on both periphyton and
phytoplankton. Three different food webs all having the phytoplankton and
periphyton, but having either one of the consumers or both were set up.
These food webs were studied in an open and closed environment. In the
open environment, phytoplankton was continuously flowing through the
aquaria, whereas in the closed envrionment all the phytoplankton was
delivered at the start of the experiment. The effect of the allochtonous input in our experiment depended
substantially on the identity of the consumer in the recipient food web. In
the absence of Daphnia (Chydorus only treatment), the biomass of
Chydorus and periphyton did not differ from the same treatment in a closed
environment. In contrast, in the presence of Daphnia, the allochtonous input
was made accessible to periphyton and hence also to Chydorus. The positive
effect of Daphnia on Chydorus was found both in the open and closed
environment. The positive effect on Chydorus relates to that Daphnia
increases the amount of nutrients for periphyton by grazing on
phytoplankton, both by decreasing the competition of nutrients from
phytoplankton, and by increasing the overall amount of nutrients through
nutrient regeneration. In the open environment, Chydorus increased to very
high numbers and was able to depress phytoplankton, and thereby negatively
affect Daphna. There was, however, no effect of Chydorus on Daphnia in
the closed environment. The contrast between the effect of Chydorus
between the open and closed environment relates to that the renewal rate of
20
phytoplankton in the open environment was independent of the grazing rate
in the recipient food web, resulting in a higher Daphnia biomass and a
higher periphyton biomass in the open environment. Our study shows how
the compensatory responses among the primary producers (increase in
periphyton) had a strong feed back effect on the consumer densities, i.e. an
increase in Chydorus which in turn lead to a decrease in Daphnia.
Allochtonous input and different food web configurations:
Responses of the microbial community ( V)
The microbial community clearly responded to the different densities of D.
pulex found in the open and closed environment (IV). As a result of the
higher densities of Daphnia, the biomass of flagellates and bacteria was
lower in the open food web configurations than in their closed counterparts.
For the ciliates, the effect could not be elucidated however. The food web
configuration also affected the results, as the lowest bacterial biomass was
found in the open Chydorus only configuration, in spite of the fact that the
biomass of ciliates and flagellates was similar to the open Daphnia
configurations. The low bacterial biomass could also not be explained by a
higher grazing on bacteria in the Chydorus treatment as Chydorus densities
were low. This suggests that the presence of Daphnia was needed to make
the allochtonous input accessible for the microbial community, probably by
regeneration of nutrients from phytoplankton to the bacteria. Our results
show that the allochtonous input had an indirect negative effect on the
biomass of the microbial community, since the inflow of phytoplankton
increased the biomass of the herbivorous cladocerans, which imposed a
higher grazing pressure on all parts of the microbial community. This result
21
differs from the traditional view that microbial biomass increases with
increasing phytoplankton concentrations.
Concluding remarks
My thesis demonstrates the importance of processes outside the focal habitat
on food web interactions within a specific habitat. These effects of the
adjacent habitat include allochtonous input of resources (I, II, IV, V), cross-
habitat foraging by consumers (II), and behaviorally induced habitat use of
consumers (II, III). My thesis also shows that heterogeneity within trophic
level can have dramatic implications for food web dynamics (I, II, III, IV).
These implications are the result of compensatory effects between two
different growth forms of primary producers (I, II, III, IV) which can
induce feedback loops between the consumers (IV). Furthermore, consumer
identity affects the way in which allochtonous resources become available to
the microbial community (V) and the herbivore food web (IV).
Previous studies have mainly viewed the littoral habitat as a source
of input of nutrients to the pelagic (Lodge et al. 1988, Schindler et al. 1996,
Schindler and Scheuerell 2002). This thesis identifies the opposite route
where 1) horizontally migrating zooplankton may exert a strong grazing
pressure on littoral phytoplankton, and 2) horizontally transported
phytoplankton may form a renewing resource base for zooplankton in the
littoral area. The pelagic zone may also function as a source consisting of
nutrient containing phytoplankton that are grazed by littoral filtering
cladocerans, whereby nutrients become available for littoral production by
periphyton. The increase in periphyton can, in turn change the dominating
22
herbivore fauna from one associated with one primary producer towards the
other (filtering herbivores toward scraping herbivores) and change the
interactions between predators within the habitat.
Ackowledgments
I would like to thank Marko Reinikainen, Pär Byström , Jens Andersson,
Karin Nilsson and Johnny Berglund for valuable comments on earlier
versions of this thesis. Finical support for this thesis was kindly provided by
The Memory of J. C Kempe foundation and The Swedish Research Council
for Environment, Agricultural Sciences and Spatial Planning (Formas) to
Lennart Persson.
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TackFörst och främst vill jag tacka min handledare, Lennart Persson, som gav migmöjlighet att doktorera. Din otroliga entusiasm, nyfikenhet och din positiva
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inställning samt din vetenskapliga briljans, har satt stor prägel på dennaavhandling. Tack för allt, Lennart!
Jens Andersson.Tack för ditt engagemang i allting. För mig har den tid som duhar varit pappaledig verkligen varit trist! Marko Reinikainen. Tack för allhjälp.Att tillbringa 90 dagar i källaren med dig, kändes verkligen inte så längesom det egentligen var, och det är till stor del din förtjänst. Pelle Byström. Tackför ditt raka och ärliga sätt samt all hjälp jag fått av dig under den tid som varit.Det har också varit ett sant nöje att ha fått vara med och se en av Sveriges bästajaktskyttar i aktion. Jocke Hjelm. Tack för all din hjälp och ditt sällskap. Detskall bli roligt att återigen få jobba ihop med dig samt att ånyo få ta del av dinkunskap om namnen på Sveriges alla växter och djur. Eva Wahlström. Tack föratt jag fick dela rum med dig. Jag har trivts och trivs väldigt bra i ditt sällskap.
Andrea Bertolo. Thank you for giving me some greate memories including thePeter Eklövs suite, dried mushrooms and all the quick Italian pasta. It wasreally a horrible summer with all the rain pouring down, but it is not the rain Iremember when I´m looking back, it is all the good laughs I had with you.
Bent Christensen, Åsa Eriksson och Frank Johansson. Tack för givande ochintressanta diskussioner om allehanda ämnen. Det är alltid ett sant nöje att fåträffa er. Thomas Brodin. Tack för de minnesvärda dagarna i Mexico näst mestromantiska stad. Johnny Berglund. Tack för ditt sällskap samt att du givit migen inblick i microbernas spännande värld! Krister Zakrisson. Tack för dinotroliga insats i sjöarna. Kjell Leonardsson. Tack för all hjälp med statistik ochförsöksdesign. Göran Andersson och Gunnar Borgström. Tack för all praktiskhjälp.
Tack Morgan och Evy Lövgren för allt ert stöd och all hjälp som jag fått. Jaghar verkligen uppskattat att ni rest 90 mil för att tillbringa en stor del av ersemester med att sy påsar till mina expriment samt att med tandborste borstasnören. Tack Olle och Anna-Lena Öhman för att jag får komma till Lövångeroch göra något annat. Tack Anna-Lena för att du tagit hand om Irma när jag harhaft mycket att göra. Tack Olle och Sture för praktisk hjälp med exprimenten.
Irma, min lilla solstråle. Vilken tur att du har hjälpt mig att tänka på annat ochgöra saker som verkligen betyder något. Tack Sara, det finns inte ord för attbeskriva den tacksamhet och kärlek jag känner för dig. Det hade aldrig gåttutand dig.
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